Loss of a biofilm-inhibiting glycosyl hydrolase during the emergence of Yersinia pestis.
Yersinia pestis, the bacterial agent of plague, forms a biofilm in the foregut of its flea vector to produce a transmissible infection. The closely related Yersinia pseudotuberculosis, from which Y. pestis recently evolved, can colonize the flea midgut but does not form a biofilm in the foregut. Y. pestis biofilm in the flea and in vitro is dependent on an extracellular matrix synthesized by products of the hms genes; identical genes are present in Y. pseudotuberculosis. The Yersinia Hms proteins contain functional domains present in Escherichia coli and Staphylococcus proteins known to synthesize a poly-beta-1,6-N-acetyl-D-glucosamine biofilm matrix. In this study, we show that the extracellular matrices (ECM) of Y. pestis and staphylococcal biofilms are antigenically related, indicating a similar biochemical structure. We also characterized a glycosyl hydrolase (NghA) of Y. pseudotuberculosis that cleaved beta-linked N-acetylglucosamine residues and reduced biofilm formation by staphylococci and Y. pestis in vitro. The Y. pestis nghA ortholog is a pseudogene, and overexpression of functional nghA reduced ECM surface accumulation and inhibited the ability of Y. pestis to produce biofilm in the flea foregut. Mutational loss of this glycosidase activity in Y. pestis may have contributed to the recent evolution of flea-borne transmission.
Erickson
David L
DL
Laboratory of Zoonotic Pathogens, Rocky Mountain Laboratories, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Hamilton, Montana 59840, USA. xenopsylla@gmail.com
Jarrett
Clayton O
CO
Callison
Julie A
JA
Fischer
Elizabeth R
ER
Hinnebusch
B Joseph
BJ
D000118:Acetylglucosaminidase / Q000235:genetics / Q000378:metabolism; D000818:Animals; D001426:Bacterial Proteins / Q000235:genetics* / Q000378:metabolism; D018441:Biofilms; D003001:Cloning, Molecular; D019143:Evolution, Molecular; D005109:Extracellular Matrix / Q000378:metabolism; D017353:Gene Deletion; D005798:Genes, Bacterial; D009699:N-Glycosyl Hydrolases / Q000235:genetics* / Q000378:metabolism; D010930:Plague / Q000382:microbiology; D011544:Pseudogenes; D005423:Siphonaptera / Q000382:microbiology; D015010:Yersinia pestis / Q000201:enzymology / Q000235:genetics*; D015011:Yersinia pseudotuberculosis / Q000235:genetics*; D047071:beta-Glucans / Q000378:metabolism
D001426:Bacterial Proteins; D047071:beta-Glucans; C505466:deacetylated poly-N-acetyl-1-6-glucosamine; D000118:Acetylglucosaminidase; D009699:N-Glycosyl Hydrolases